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Abstract
Background and Aims
Forest tree saplings that grow in the understorey undergo frequent changes in their light environment to which they must adapt to ensure their survival and growth. Crown architecture, which plays a critical role in light capture and mechanical stability, is a major component of sapling adaptation to canopy disturbance. Shade-adapted saplings typically have plagiotropic stems and branches. After canopy opening, they need to develop more erect shoots in order to exploit the new light conditions. The objective of this study was to test whether changes in sapling stem inclination occur after canopy opening, and to analyse the morphological changes associated with stem reorientation.
Methods
A 4-year canopy-opening field experiment with naturally regenerated Fagus sylvatica and Acer pseudoplatanus saplings was conducted. The appearance of new stem axes, stem basal diameter and inclination along the stem were recorded every year after canopy opening.
Key Results
Both species showed considerable stem reorientation resulting primarily from uprighting (more erect) shoot movements in Fagus, and from uprighting movements, shoot elongation and formation of relay shoots in Acer. In both species, the magnitude of shoot uprighting movements was primarily related to initial stem inclination. Both the basal part and the apical part of the stem contributed to uprighting movements. Stem movements did not appear to be limited by stem size or by stem growth.
Conclusions
Stem uprighting movements in shade-adapted Fagus and Acer saplings following canopy disturbance were considerable and rapid, suggesting that stem reorientation processes play a significant role in the growth strategy of the species.
INTRODUCTION
In many tree species, saplings may modify their crown architecture along natural light availability gradients, with a tendency to develop more horizontal and thinner stems and branches when growing under shade than under high light (; Valladares and Niinemets, 2007). This light-induced plasticity in crown architecture results from the simultaneous optimization of different processes that all vary with the light regime, e.g. light capture, maintenance of mechanical stability, water transport, resistance to pathogens and herbivory or reserve storage (Paquette et al., 2007; ). In forest stands undergoing natural regeneration, light availability strongly varies on spatial and temporal scales, and sapling acclimation to both types of heterogeneity has been recognized as a key element of their ability to access upper canopy layers and persist in the future stand (Canham, 1988). However, variations in crown architecture in response to changes in light availability have mostly been studied on saplings growing in contrasted but stable light regimes, and the effects of temporal changes in light availability on the morphology of sapling crowns remain largely unknown (Kneeshaw et al., 1998; Zenner, 2008).
In forests characterized by intermediate disturbances, where recruitment generally occurs in canopy gaps, successful trees often experience multiple canopy opening and closure episodes before reaching the upper canopy layer (Webster and Lorimer, 2005). During canopy closure phases, the trees must persist for long periods under low light, thus developing a shade-adapted morphology. When released, they must rapidly acclimate to their new conditions to take advantage of the higher light intensity and therefore need to adopt a sun-adapted morphology. For species that exhibit a more plagiotropic shoot development in shade than in sun conditions, these morphological changes imply a vertical reorientation of the stem (Hamilton et al., 1985). Vertical stem reorientation may result from different processes, which have been shown to occur in young trees in response to various environmental stimuli.
(a) Vertical stem reorientation may result from a replacement of plagiotropic leader shoots by more vertical relay shoots. The reiteration process is the development of a branching system resulting from the activation of dormant buds or from the de-differentiation of a branch shoot that repeats the architectural sequence of the parent shoot in response to an increase in resource availability, to damage to the leader shoot or to a loss of vigour of the leader shoot (; Bell, 1991). The development of reiterated shoots that relay the initial leader shoot plays a significant role in the growth strategy of many tree species at the sapling stage by promoting sapling survival under a variety of stressful conditions, including suppression by canopy trees (Del Tredici, 2001).
(b) Vertical stem reorientation may result from a change in the growth direction of the elongating part of the stem towards a more vertical upright direction. Changes in the growth direction of elongating shoots resulting from differential cell elongation in the shoot apex have been documented across a wide range of plants species in response to shoot bending or to changes in the light environment (; ).
(c) An uprighting movement of the lignified part of the stem may also lead to vertical stem reorientation. Radially growing woody stems that have finished elongation can actively bend by asymmetrical formation of reaction wood and normal wood around the stem (Fournier et al., 2006). Asymmetric wood maturation has been shown to be the main mechanism involved in gravi-autotropism (), a process by which the tree may regulate its posture or may recover from mechanical injuries such as moderate windthrow, soil slipping or buckling under its own weight (). Stem uprighting caused by asymmetric wood maturation has been shown on tree seedlings grown in pots in response to pot inclination (; ), but has rarely been studied on young trees growing under natural conditions. Bending may occur along the entire tree stem from base to apex, but the relative contribution of the different parts along the stem to whole plant movements has not yet been described. Towards the stem base, the potential for bending movements is progressively restricted by the increase in diameter. However, since basal movements drive movements of upper plant parts, even slight bending at the stem base has significant effects on whole plant posture. Biomechanical models have shown that the magnitude of bending movements in lignified shoots is limited by initial shoot inclination and diameter and by radial growth ().
The objectives of this study are (a) to test whether tree saplings that have grown for long periods under a closed canopy and that have developed shade-adapted crown architecture display vertical reorientation of stems in response to canopy opening; (b) to identify the morphological features that cause vertical stem reorientation (uprighting movement of the stem, changes in stem apex growth direction, or formation of relay shoots) and to quantify the contribution of stem base reorientation to whole plant reorientation; (c) to test whether stem vertical reorientation after canopy opening is related to sapling morphology measured before canopy opening (stem inclination and diameter).
A 4-year-experiment was conducted under natural conditions to analyse potential morphological adjustments of shade-acclimated Fagus sylvatica and Acer pseudoplatanus saplings, in response to artificial canopy gaps. Fagus and Acer have been shown to form an abundant sapling bank under a closed canopy that reacts positively and rapidly to canopy opening (Caquet et al., 2010).
MATERIALS AND METHODS
Study site and plant material
The study was conducted in the Graoully forest (49°04′N, 06°01'E) in the Lorraine region, north-eastern France, on a limestone plateau at approx. 300 m asl. The long-term annual average temperature was 10·1 °C and average annual precipitation was 745 mm. Soil characteristics (a 40- to 60-cm-deep calcisol) were homogeneous over the whole site and the study area was flat. The stand had been managed under a coppice-with-standards regime until the beginning of the 1960s when the conversion into high forest began. As of that date, harvesting of the coppice stopped and only a few sanitary thinnings were performed. In 2004, the mature stand was dominated by Fagus and Carpinus betulus. An abundant natural regeneration dominated by Fagus and Acer was present below the canopy in most of the stand (Collet et al., 2008).
In June 2004, a 400-m2 square plot containing 0·1- to 3-m-high advance saplings of the two species was selected. In January 2005, felling was carried out to create a canopy gap above the plot. In summer 2004 and 2006, hemispherical photographs were taken with a digital camera (Coolpix 5000 with a FC-E8 fish-eye lens, Nikon Corporation, Tokyo, Japan) at a height of 1·50 m on a 4 × 4 m grid in the plot. Saplings higher than 1·50 m were manually moved away from the camera so that only the adult canopy appeared on the photographs. Photographs were manually thresholded to a black and white image, and relative irradiance was calculated for each photograph using HemIMAGE software (Brunner, 1998). Relative irradiance ranged between 3 % and 6 %, and between 25 % and 39 % before and after canopy opening, respectively.
In December 2004, 0·5- to 2·5-m-high saplings (32 Fagus and 22 Acer) were selected for measurement. Height was used as a stratification variable: height range was divided into three equal-size height classes and, for each species, a similar number of trees was selected in each height class. More Fagus saplings were selected because they had, on average, more lateral branches and exhibited a larger variation in their branching pattern than Acer saplings. During the 4 years of the experiment, one Fagus and six Acer saplings died. Analyses were performed only on the saplings that survived, i.e. 31 Fagus and 16 Acer. In 2004, sapling height ranged between 0·64 and 2·34 m and between 0·74 and 2·49 m, basal diameter between 0·9 and 2·4 cm and between 0·7 and 1·9 cm for Fagus and Acer, respectively. Height and diameter values were evenly distributed along the sampled range of values for each species. Individual height and diameter were positively and linearly related, using the same relationship for the two species (height = 0·32 + 0·82Diameter, adj-R2 = 0·62, n = 47, species not being significant when introduced as additional variables into the model). Sapling age in 2004 (estimated at the end of the experiment by counting the annual rings on a stem section cut at the sapling base) was 18·9 ± 0·85 (10–31) years and 21·1 ± 0·93 (15–28) years for Fagus and Acer, respectively [mean ± s.e.m. (min–max)]. On average, larger saplings were older although the correlation between age and size was weak (Fagus: age = 6·70 + 7·58 Diameter, adj-R2 = 0·40; Acer: age = 13·6 + 5·97Diameter, adj-R2 = 0·31). Consequently, for each species, age variability among saplings in any height or diameter class was large.
The distance between selected saplings was at least 2 m. All other tree saplings growing in the plot were cut down at the beginning of the experiment and the plot was manually weeded each year throughout the experiment to avoid any potential interaction with neighbouring plants.
Growth measurements
From 2004 to 2008, the saplings were measured each year in December. Sapling basal diameter was measured at 5 cm above the ground using a digital caliper. The main axis was considered to be the sapling's highest axis, and marks were painted every 20 cm along the main axis. The location of the marks along the stem was determined using a soft tape. The inclination of each of the successive 20-cm-long segments along the axis was defined as the angle relative to a horizontal plane and was measured with an electronic inclinometer. The length of the last segment (often <20 cm) was measured in addition to its inclination. Segment azimuths were not measured. Axis length (defined as the sum of the individual segments along the axis) and sapling height (height of the axis apex above ground surface) were computed from individual segment lengths and inclinations.
For saplings whose main axis changed between two successive measurement dates as a consequence of the rapid growth of a lateral axis, the change in dominance was recorded and measurements were performed on both the relay axis (defined as the new main axis) and the former main axis. On one sapling, the main axis changed twice during the experiment and measurements were made on the three axes the last year. When a relay axis was recorded, its position along the former main axis and its age (year of appearance on the former main axis) were estimated. The main axis defined in 2004 (beginning of the experiment) was referred to as axis 1.
Computation of geometric descriptors
Since the azimuths of the axis segments were not measured, sapling geometry was defined and analysed in a vertical plane (2-D).
On each sapling, angle xOA0 where A0, is the location of the apex (at the base of the apical bud) of axis 1 in 2004 and which reflects initial sapling inclination, was computed (Fig. 1A). For each measurement year from 2005 to 2008, three angles were defined and computed:
(1) angle xOA, where A is the location of the scars of the 2004 winter bud on axis 1, which reflects up- or downrighting movements of axis 1, when compared with angle xOA0;
(2) angle xOE, where E is the apex of axis 1, which reflects changes in the inclination of axis 1 as a result of combined up- or downrighting axis movements and axis elongation since 2004, when compared with angle xOA0;
(3) angle xOR, where R is the apex of the main axis, which reflects changes in sapling inclination as a result of combined up- or downrighting movements of axis 1, elongation of axis 1 and the appearance of a relay axis, when compared with angle xOA0. For saplings with no relay axes, R = E (axis 1 is still the main axis).
Angle definition. (A) Angles used to describe axis inclination. The sapling in 2004 (with axis 1 as the main axis) is drawn in black, and the sapling in 2008 is drawn in grey (with axis 1 as the former main axis, and axis 2 as a relay axis that appeared in 2007). A0 is the location of the apex of axis 1 in its initial position (in 2004), A is the location in 2008 of the scars left by the 2004 winterbud, E is the location of the apex of axis 1 in 2008, and R is the location of the apex of the main axis in 2008 (in the present case, a relay axis). Saplings are represented in a vertical plane and for all angles the baseline is the horizontal line (O, x). (B) Observed and simulated inclination of axis 1. B and B0 are the location of the limit between the base (0–80 cm) and the upper part (above 80 m) in 2004 and 2008, respectively. Abase is the location of the apex of axis 1 that would be reached in 2008 if only the base bent (i.e. if no bending occurred in the upper part). In the upper part of the axis, the angles between two successive 20-cm-long segments are indicated. On the axis in 2004, angles a, b, c and d are directly computed from the measurements. On the axis simulated in 2008, the same angles are reported to show the lack of bending movements in the upper part.
For each species and for each year, the three angles were compared with angle xOA0 using Student's paired t-tests. To relate up- and downrighting movements of the main axis over the 4 years to initial sapling characteristics, the relationship between angle A0OA (calculated from angle xOA and angle xOA0) and initial sapling characteristics was analysed using linear models, according to:
where xOA0 is the initial inclination, Size is the initial height or diameter, Growth is the height or diameter increment over the 4 years, and Species is the species concerned. The significance of each independent variable was tested using ANOVAs.
An index of stem straightness was calculated for each sapling:
where I is the straightness index, Length is the length of axis 1 and Chord is the length of the chord between the root collar and the apex. An index of 0 indicates a straight (but possibly leaning) axis, and higher index values indicate less straight axes.
To assess the importance of righting movements of the basal part of axis 1, which may drive movements of the upper part of the axis, curvature in the basal part of axis 1 was defined and changes in curvature over the 4 years were calculated. Local curvatures are the rate of changes in inclination with position along the stem per unit length (for more details, see ). Thus, mean curvature at the stem base (0–0·8 m stem portion) was estimated as the slope of the linear regression of the first four inclination measurements versus their average position along the stem (with position expressed in metres and angle in radians, to obtain curvature in m−1). Changes in basal curvature between 2004 and 2008 were analysed for all saplings excluding three Acer where a relay axis appeared below 0·8 m.
In a second step, angle xOAbase, defined as the angle xOA that would be observed if only the axis base bent (i.e. if no bending movement occurred in the upper part (above 0·8 m) of axis 1, Fig. 1B) was calculated as:
hence
where ΔC is the variation of the mean basal curvature from 2004 to 2008, L the mean base length (L = 0·8/2 = 0·4 m), with angles in degrees and ΔC in m−1.
In addition, in Fagus, to compare movements in basal and in upper parts, curvatures were also estimated from the inclination of the four segments located between 0·8 and 1·6 m. This value was estimated on all Fagus, excluding six saplings that were too small or that had a relay axis below 1·6 m. It could not be done on Acer because relay axes were frequent and too few saplings were available.
Finally, to represent the vertical movements of axis 1, an average sapling was computed each year for each species. For each measured sapling and for each year, the co-ordinates (x, y) of ten points equally spaced along the axis were computed. The mean of these co-ordinates was computed and used to draw an average sapling for each year and each species.
Computation of gravitropic efficiency from curvature variations
proposed general mechanical formulations to model the gravitropic efficiency of righting movements of radially growing stems. These formulations show how size (initial diameter), growth (cambial and biomass growth) and the asymmetry of wood characteristics (bending stiffness and maturation strains induced during wood lignification) physically interact to bend the stem. They may be used to define the gravitropic efficiency of the righting process, as an individual and local (defined along the stem) variable, based on curvature variation measurements and physically independent of size and growth. The simplest model (Fournier's model, according to ) was used as follows:
where D is the basal diameter (D0, initial basal diameter in 2004) and C the curvature (C0, initial curvature in 2004) at a given height, and e is the gravitropic efficiency, i.e. a non-dimensional factor that depends on reaction wood quality and on the form and the heterogeneity of the cross-section, independently of stem size and radial growth. Following this definition, gravitropic efficiency is comparable to the efficiency defined by and or to the apparent efficiency defined by .
RESULTS
Sapling growth and relay shoot development
For both species, sapling diameter increased each year from 2005 to 2008 (Fig. 2). Sapling height for Fagus also increased each year, whereas for Acer, it remained stable for 2 years and strongly increased afterwards.
Sapling height and diameter (mean ± s.e.m.) for Fagus sylvatica and Acer pseudoplatanus saplings after canopy opening.
One Fagus and six Acer individuals had a relay axis in 2007, and two Fagus and five Acer in 2008. One Acer sapling changed both in 2007 and 2008, thus giving a total of three out of 31 selected Fagus and ten out of 16 selected Acer, which changed during the 4 years of the experiment. Among these relay axes, two and four axes already existed as small branches in 2004 and one and seven axes appeared later (in 2007 or in 2008) for Fagus and Acer, respectively. All the relay axes were located on the portion of axis 1 elongated before 2004.
Sapling vertical reorientation
Initial sapling inclination (expressed by angle xOA0) ranged from 40° to 71°, and from 56° to 75°, with average values of 58° and 68° for Fagus and Acer, respectively (Fig. 3). For Fagus, angle xOA increased progressively to reach an average value of 76° in 2008, and angle A0OA was significantly different from 0 in all years. For Acer, angle xOA decreased for 2 years, and then strongly increased to reach an average value of 75° in 2008. For Acer, angle A0OA was significantly different from 0 only in 2008. Over the 4 years of the experiment, all Fagus showed uprighting stem movements (lowest value: +3·6°), whereas three Acer showed downrighting movements (lowest value: –7·3°).
Axis inclination (mean ± s.e.m.) for Fagus sylvatica and Acer pseudoplatanus saplings after canopy opening. Angles xOA, xOE and xOR are defined in Fig. 1. In 2004, all angles are equal to xOA0. For each species, each angle and each year from 2005 to 2008, the result of a paired t-test comparing the angle to xOA0 is indicated (*, significant at α = 0·05; n.s., non-significant). The arrows indicate the contribution of the three processes (stem uprighting movements, stem elongation, appearance of relay axes) to total sapling stem reorientation over the 4 years of the experiment.
ANOVAs performed on linear models expressing angle A0OA as a function of initial inclination, initial size, growth and species showed that angle xOA0 was the only variable that significantly affected angle A0OA. For both species, the model A0OA = 68·4 – 0·88 xOA0 was selected (n = 46, P-value < 0·001, adj-R2 = 0·49), indicating that the largest uprighting movement occurred for the lowest initial inclination.
Compared with angle xOA, angle xOE was slightly lower for Fagus and slightly higher for Acer. Angle AOE, which reflects the contribution of primary growth to potential axis vertical reorientation, was always small (<2°, in absolute values).
Since relay axes did not appear before 2007, angle xOR was equal to angle xOE until 2006 for all saplings. In 2007 and 2008, angle EOR was approx. 1° and 5° for Fagus and Acer, respectively. Angle EOR was positive for all saplings.
Mean variation in basal curvature between 2004 and 2008 was 0·25 m−1 and 0·40 m−1 for Fagus and Acer, respectively. No statistically significant differences occurred between the two species, and there was no correlation with the growth × size factor [(1/D0) – (1/D)].
Curvature estimated in the upper part of the stem (at a height of 1·2 m) in Fagus showed higher variations than at the stem base (mean = 0·58 m−1), significantly correlated with the growth × size factor (n = 24, adjusted R2 = 0·37, P-value < 0·001).
Figure 4 shows the contribution of vertical movements in the axis base to whole axis movements over the 4-year period. In Fagus, movements in the basal part accounted for approximately one-third of the righting movement of the whole axis (mean A0OAbase = 5·8°, mean A0OA = 18°). In Acer, basal movement was a major contributor to whole axis movement (mean A0OAbase = 9·2°, mean A0OA = 7°) and, for half of the saplings, basal movement was even greater than the righting movement of the whole axis.
Contribution of basal (0–80 cm) uprighting movements to total stem movement in Fagus sylvatica and Acer pseudoplatanus saplings: simulated angle xOA (angle that would be observed if only the axis base bent = xOAbase) in relation to xOA measured in 2008. Each point represents a sapling. Points below the identity line denote saplings where basal movements contribute to a small part of total stem movements. Points above the identity line denote saplings where an autotropic overcorrection process occurs.
Figure 5 shows the average shape of axis 1 for Fagus and Acer saplings. In Fagus, the progressive uprighting movement previously quantified in Fig. 2 is clearly visible. In Acer, axis 1 showed a (non-significant) downrighting movement during the first 2 years and an uprighting movement afterwards (significant only in 2008). In Fagus, uprighting movements were greater in the apical than in the basal part of the axis, leading to an increase in axis straightness from 2004 to 2008 [mean (s.e.m.) straightness index = 7·31 (0·49) and 0·91 (0·14) in 2004 and 2008, respectively]. Acer was slightly straighter in 2008 than in 2004 [mean (s.e.m.) straightness index = 2·49 (0·41) and 1·52 (0·21) in 2004 and 2008, respectively]. Axis 1 was straighter in Acer than in Fagus in 2004 but the opposite was observed in 2008. These differences were statistically significant, as shown by t-tests comparing the straightness index in the two species (P-value < 0·0001 and P-value = 0·021 in 2004 and 2008, respectively). Figure 6 shows photographs of two individual saplings that illustrate these changes.
Average shape of axis 1 from 2004 to 2008 for Fagus sylvatica and Acer pseudoplatanus saplings after canopy opening (see text for calculation of the average axis shape). Axis 1 was selected as the main axis in 2004 and was still the main axis in 2008 for 28 (out of 31) Fagus and six (out of 16) Acer.
Photographs of an Acer pseudoplatanus and a Fagus sylvatica sapling in 2004 and in 2008. For each species, the two photographs represent the sapling from the same point of view and at the same scale. Photographs: Michel Pitsch and Thiéry Constant.
Gravitropic efficiency
Basal gravitropic efficiency ranged from –1·2 to 6·2 mm m−1, with a mean value of 1·6 mm m−1. As expected from the lack of correlation between curvature and the growth × size factor, gravitropic efficiency was highly variable among individuals and there was no significant difference between the two species. In Fagus, efficiency was less variable in the upper part (CV = 68 %) than at the stem base (CV = 120 %).
There was a significant interaction between species and initial inclination (adjusted R2 = 0·23, ANOVA, P-value = 0·004), but no effect of initial size and growth on the efficiency at the base of the stem. For each species, efficiency was correlated with initial inclination (highest efficiency for biggest angle xOA0), the effect of inclination being significant for Fagus (P-value < 0·001) but not for Acer (P-value = 0·4).
In Fagus, efficiency estimated in the upper part was not correlated to any factor.
DISCUSSION
Uprighting movements are large and rapid
Shade-adapted Fagus and Acer saplings responded dramatically to canopy opening and showed a rapid increase in diameter growth and a regular increase in height growth, corroborating previous work on the two species (Caquet et al., 2010; Collet et al., 2001). They also showed strong stem reorientation (18° in Fagus and 15° in Acer).
The uprighting movements of the lignified stem were large and came with significant variations in stem curvature. Gravitropic efficiency fell within the range 0–15 mm m−1; previously observed for others tree species [Populus sp. (), Pinus pinaster () and eight tropical tree species ()] in greenhouse experiments with saplings grown in pots and where initial inclination was controlled. When comparing these greenhouse tilting experiments to the present experiment, the initial sapling inclination and the observed efficiencies have similar values, although the stimuli acting on the saplings strongly differ between the two experiment types (gap opening versus artificial tilting).
Since the work of Hamilton et al. (1985), this is the first study showing the ability of tree saplings to become more erect in response to a change in their growth environment. Contrary to previous greenhouse pot experiments where the saplings were tilted, the saplings in the present experiment were not manipulated and only external factors (canopy opening) were changed. However, the saplings responded as rapidly and as strongly as in experiments where saplings were physically handled. The similarities in sapling response between the present experiment and greenhouse experiments constitute a validation of the hypothesis that tilting experiments may effectively be used to estimate the behaviour of saplings grown under natural conditions.
The magnitude of the uprighting movement observed after gap opening was impressive and was not species-specific, although Fagus and Acer had been selected for their contrasting crown architectures. The magnitude, the rapidity and the generality of stem straightening observed among the study saplings strongly suggest that the process plays an important part in the ability of saplings to respond positively to canopy opening.
Processes involved in the uprighting movement differ between species
In both species, annual sapling vertical reorientation and annual height growth were closely related. In Fagus, both processes started immediately and progressively increased after canopy opening, whereas in Acer both processes were delayed for 2 years and rapidly increased afterwards.
In both species, stem reorientation occurred mainly through uprighting movements of the lignified stem, accounting for 93 % and 48 % of the process in Fagus and Acer, respectively. In Acer, the appearance of relay axes and elongation of the main stem also played a major role, accounting for 33 % of total stem reorientation and for two-thirds of the saplings, in agreement with previous knowledge about the ability of Acer to produce relay shoots. In Acer, a third important process was stem elongation that accounted for 18 % of total stem reorientation. As described by Bell (1991), Acer has a vertical shoot growth direction, which explains the contribution of shoot elongation to the reorientation process. On the contrary, in Fagus uprighting movements were the main process accounting for stem reorientation; appearance of relay axes accounted for only 7 % of total stem reorientation, and stem elongation actually reduced vertical reorientation by 6 %, in agreement with the plagiotropic growth direction of its stem apex (Peters, 1997).
Local focus on basal curvature supported the analysis performed at the axis level, since basal movements accounted for a large part of whole axis movements. Interestingly, in Acer, basal movements were often larger than whole stem movements, indicating an overcorrection of the apical part of the stem. This process, usually referred to as autotropic movement (), compensates for a basal movement that would be too rapid. The overcorrection, usually associated with oscillatory curvatures and movements, resulted in a less straight final form of Acer as compared with Fagus. These observations are in agreement with who suggested that poor stem form should be associated with fast uprighting movements. Acer developed a more complex regulation of stem verticality that combined many processes (elongation, relays, stem bending) with gravi- and auto-tropism to co-ordinate them. Fagus, although initially more horizontal, mainly used gravitropic reaction wood formation to reach a more vertical posture.
Stem uprighting is not strongly limited by size and growth
Biomechanical models suggest that posture control is highly constrained by size (). Stems with larger diameters are more difficult to bend and the effect is not compensated for by the higher gravitropic efficiency and greater growth observed with diameter, within a wide range of diameter values. Uprighting movements are therefore supposed to be limited by stem diameter. In the present experiment, stem response was obviously not limited by size or growth: the magnitude of uprighting movements of the whole stem (analysed in terms of both angles and efficiencies) depended mainly on sapling inclination before canopy opening, lean saplings showing, on average, larger uprighting movements (24° on average for a sapling with an initial inclination of 50°), leading to smaller variations in stem inclination among the saplings 4 years after canopy opening than before canopy opening.
In Fagus, movements in the upper part of the stem accounted for two-thirds of total stem uprighting movements. Contrary to what was observed at the stem base, uprighting in the upper part of the stem seemed to be close to its geometrical limit, as suggested by the correlation between curvature and the growth × size factor and by the lack of significant effect of initial inclination on efficiency. In the upper part, stem reorientation capacity seemed to be saturated and was limited by stem diameter and radial growth.
The reorientation process was still rapid at the end of the experiment for both species, and questions still remain about the maximum values of stem reorientation that saplings may reach and about the temporal dynamics of the process over longer time periods (5–10 years).
Growth strategy of Fagus and Acer saplings
Fagus and Acer are known for their shade tolerance and their ability to form a persistent sapling bank under closed-canopy conditions (Hein et al., 2008, Wagner et al., 2010), where sapling age usually ranges between 1 and 35 years (Collet et al., 2008). Under closed-canopy conditions (relative irradiance below 5 %), height growth is very low (usually <2 cm per year) for both species, and Acer rarely exceeds 1·5 m in height, whereas Fagus often reaches several metres (Ammer, 1996; Nicolini et al., 2001). Following partial or full canopy removal, Fagus and Acer advance regeneration resumes rapid growth and may dominate regeneration within a few years (Wohlgemuth et al., 2002; Nagel and Diaci, 2006). Descriptions of the architecture of saplings growing under a closed canopy have shown that Acer usually has many scars of apical die-back, related to herbivory or shoot desiccation (Gardère, 1995). Apical die-back also occurs in Fagus, although much less frequently (Nicolini and Caraglio, 1994). Many studies have reported strong stem inclination for Fagus saplings growing under a closed canopy (von Lüpke, 2005) but such information is lacking for Acer. The present study shows that under similar closed-canopy conditions, Acer is less plagiotropic than Fagus. In addition, it shows that after canopy opening, Acer sapling height remains stable for 2 years, increases rapidly afterwards and catches up after 2 more years with Fagus height, which increases at a lower but steadier rate.
The present experiment was part of a larger study (Collet et al., 2008; Caquet et al., 2010) that investigated the dynamics of naturally regenerated Fagus and Acer saplings growing in stands submitted to periodic intermediate disturbance, where trees often experience several canopy opening and closure episodes before they reach the upper canopy (Canham, 1988, Webster and Lorimer, 2005). When taken with previous knowledge, all these findings suggest different height growth dynamics for Fagus and Acer saplings and different growth strategies for the two species.
In Acer, after canopy closure, height growth is strongly reduced and saplings undergo multiple stem die-backs. After canopy release, stem height growth often starts from a lower point on the stem. For most saplings, part of the height they acquired in a canopy opening episode is lost during the next closed-canopy period. However, the height loss is balanced by the rapid growth rate after canopy opening, enabling Acer to outcompete other saplings. Under shade, diameter growth is also restricted and Acer saplings do not develop much supporting tissue. However, since sapling height is restricted and Acer architecture is more orthotropic, mechanical buckling is avoided and reorientations in the stem base are efficient to maintain the required verticality. The low stem diameter is a factor that ensures security by increasing reorientation capacity. After canopy opening, many processes converge to increase verticality: relay axes, primary orthotropic elongation and stem gravitropic and autotropic reorientation by secondary growth. Redundancy in posture control processes allows the saplings to respond rapidly to canopy opening and, in addition, to respond positively to other potential disturbances such as herbivory or mechanical damage.
In Fagus, fewer stem die-backs occur during closed-canopy episodes, and relay axes appear only on a small number of saplings after canopy opening, thus limiting sapling height losses. Maintenance of sapling height during long periods of canopy closure enables Fagus saplings to maintain their dominance over potential neighbouring competitors after canopy release, despite low height growth rates. The ability of Fagus saplings to maintain, under shaded conditions, the height they acquired in previous periods of high light availability, enables them to take advantage of multiple canopy closure and release episodes. In the shade, diameter growth is reduced while stem height is maintained, leading the stem to bend under its own weight. After canopy opening, long annual shoots develop at the apex of the existing stem, strongly increasing stem load and requiring rapid stem uprighting movements to avoid buckling. Uprighting is achieved through local movements that occur along the whole stem.
Conclusions
Uprighting movements of the lignified stem have been reported in many studies where tree seedlings were tilted under controlled conditions (; ; ). The present experiment provides clear evidence that the processes described in these pot studies also occur in young trees growing under natural conditions, and that the observed effects are of similar magnitude and time scale.
The magnitude and the rapidity of stem reorientation processes in shade-adapted saplings following canopy disturbance suggest that it is a major feature of the growth strategy of Fagus and Acer. For both species, stem reorientation is necessary to prevent the stem from bending during growth.
Stem reorientation efficiency is known to be size limited. Thus, if gravitropic performance is a key process determining sapling ability to respond positively to canopy opening, saplings growing under a closed canopy must remain under a size threshold where gravitropic performance is not limited. The present study shows that Fagus and Acer saplings have good gravitropic performance up to 2 m, a height sufficient to provide saplings with a decisive advantage over potentially competiting neighbours.
In Fagus, large uprighting movements are associated with a conservative strategy where sapling height is maintained throughout the duration of the closed-canopy phase. In Acer, formation of relay axes is associated with a less-conservative strategy where sapling height losses occur and are counterbalanced by higher growth rates after canopy opening.
ACKNOWLEDGEMENTS
We thank Christopher Baraloto and anonymous reviewers for helpful comments on the manuscript. This work was supported by the Regional Council of Lorraine (‘Jeune Equipe 2005′), Office National des Forêts (‘ModelFor’ project) and INRA (‘Forêts mélangées’ project within the ECOGER programme).
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A brand-new Windows computer should be pristine out of the box. After all, you haven't gummed it up yet with software, right?
Leave that to the computer manufacturers. They'll gum it up for you with 'free' software you don't want. It goes by names like crapware, bloatware, or shovelware because computer makers shovel bloated digital crap by the barrelful onto new PCs. There's a reason for that-crapware offsets the price of super-cheap PCs on retail shelves, even if it's only by pennies.
I'd never had major problems with crapware when buying PCs via mail order. But in retail, it's a whole other world of crap. For example, a few years ago, my technophobic father, then age 75, got a new PC to replace his dying Windows Vista system, which he mainly used to print pictures. I couldn't really recommend spending a lot of money to get it fixed. 'Just go find an off-the-shelf for under $400, it'll be fine compared to what he's got,' I told my mom (aka Dad's IT person in residence).
Hardware-wise, that Acer Aspire X (Model AXC-605G-UW20) they purchased at Walmart was sufficient. The specs all qualified as an upgrade.
To get that price of $399, however, Acer sold out my parents and wasted hours of my family's lives to fix it.
Using TeamViewer remote control software, I saw the system was a mess, yet all Mom had done was install the software for Dad's beloved (yet dying) Kodak printer. The desktop was awash in at least 15 icons for needless, worthless crap. Opening up the Uninstall a Program control panel revealed even more in residence. Mom tried to uninstall the obvious things, but they persisted.
With many of the uninstall routines, the dialog boxes had giant buttons that would say 'Uninstall and Get PC XXXXXX' or something similar. If we just wildly clicked where the button was, the uninstall might work-but something else got installed in its place. We had to carefully look for the fine print on the dialog boxes that read 'Delete Only' or similar. Tricks and traps abounded.
Back then, I turned to Slim Computer from Slimware Utilities. It appears to have been discontinued, but at the time it kept a database of crapware and helped identify it on a new Windows PC. With it gone, another option is the excellently named PC Decrapifier as well as Should I Remove It?
The problem is, even though these utilities may point out some bloatware, they may not automate removal. You may still have to go through the regular uninstall process, which-as we noted above-may be filled with tricks and traps to keep your new PC full of crap. So you may still be on your own to an extent, but there are ways around it.
'Potentially Unwanted' Crap
Dad's new Acer PC also had actual malware in the guise of 'potentially unwanted programs,' or PUPs.
The programs don't call themselves that; it's a term used by anti-malware companies, like MalwareBytes. It describes programs you probably didn't install on purpose, don't want, and probably find unusable-but they have to say 'potentially' because, sure, it's possible you wanted to install a toolbar for your browser called 'Search Protect' from a company named Conduit, or a search engine for your browser called Binkiland.
In reality, it's about as likely as wanting to be set on fire. Both of those 'programs,' among others, were on my dad's PC. They existed only to take over his browsing experience; each appears on a list of browser hijackers on Wikipedia.
Others you may see and should eradicate immediately: Taplika, SwiftBrowse, BetterSurrf, CrossRider, WeDownload, OpenCandy, OptimizerPro, and DoSearches. The list can and will go on and on, as the hijackers make new threats. It's telling that searching for 'Search Protect' or 'Binkiland' brings up absolutely no link for people to get those programs-only to remove the damnable hijackers' files.
The hijackers did a number on my dad's PC. I couldn't get the installed browsers (IE and Firefox) to go to a web page to download new tools to deal with these threats. I had to download the clean-up software to my workstation, then use TeamViewer to do a remote file transfer of the EXE installer to dad's desktop.
Also note that at this point, we uninstalled McAfee Security Suite, which came free with the Acer as well. You may not consider antivirus software as shovelware, but it certainly can be. Acer didn't put it on there to be altruistic; McAfee paid for placement. Plus, McAfee was likely to 1) slow the PC more than smaller, free AV products we could install later and 2) would eventually cost $79 after the trial was over. No thanks.
Here's a rundown of the tools we used to clean the hijacking PUPs:
- MalwareBytes: The free version comes with a trial of the Premium version, so it's worth running on every fresh installation of Windows. Plus, the scans take a lot less time on a new Windows install. After 14 days, you lose things like real-time protection and anti-ransomware features, but it's worth running up front. Remember after that two weeks, get some real-time anti-malware protection.
- Steven Gould's Cleanup!: Donationware that does the trick for Windows XP on up.
- CCleaner: This Windows clean-up tool will do something unique: it'll uninstall apps built into Windows. I'm not talking shovelware crap, but actual apps that Microsoft created to work with Windows-so consider it OS-sanctioned crapware. Click on Tools, then uninstall, and you'll get a list of possibilities to delete. (This suggestion might be controversial: now owned by Avast, CCleaner got hit with from makers like HP, Razer, Sony, Toshiba, Dell, MSI, Asus, Acer, and Lenovo. Custom-build manufacturers that promise you a crapware-free installation of Windows include Maingear, Falcon Northwest, and Velocity Micro. Another option: go with a local reseller.
Or, buy a Mac or a Chromebook and avoid Windows altogether.
If you want to save money, install Linux on your old PC. (That wasn't really an option for my father.)
If you're wedded to using an older version of Windows, the only sure-fire way to get the same result is re-install Windows completely, with a totally fresh, clean configuration. That's not possible with most retail PCs that had Window 7, 8, or 8.1. Whether the operating system installer is an image on a partition of the hard drive or a DVD disc, it's going to most likely install Windows with all the crapware, fresh as an outhouse, as well. If you can't keep a retail copy of Windows 7 or 8 around for reinstalls, it makes the update to Windows 10 seem even more advantageous. You can even do the refresh and not lose your data files on well-used PCs.
There's the option to download ISO files of Windows 7 and 8 and even 10 at the Microsoft Software Recovery site. You'll need to verify a 25-character product key from a retail version of Windows to download and fully activate the operating system. Keys from computer makers-called OEMs, or original equipment manufacturers-won't work.
Why Is This Happening?
You might be wondering, why exactly are big-name PC makers and software developers allowing all this crapware with extra 'internet wrappers' PUPs to happen? Money, of course. As PC sales dwindle-they were on a five-year slump through 2017, but had a slight uptick over the holidays-so do software purchases, and everyone is scrambling to make up for any losses.
For proof, look to this article by How-To Geek. They examined programs from every single major download site, including CNET's Downloads.com, Tucows, FileHippo, Softpedia, Snapfiles, and more. Every single one had crapware bundled right into the software. That's not even taking into account that some of those sites have multiple download 'buttons' (actually ads) on every page, to obfuscate and confuse users into downloading the wrong thing.
Always download software from the original developer's site (if you can find it). Unfortunately, even Google search results tend to default to download sites like those listed above.
Pundit Ed Bott once called for a PC 'Truth in Labeling Act' to force the PC manufacturers to tell users what's pre-installed. It's an excellent idea that will never happen. It would be nice if the download sites, some of which claim they don't allow any type of malware, would do the same.